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The Journal of Neurophysiology Vol. 83 No. 5 May 2000, pp. 2956-2966
Copyright ©2000 by the American Physiological Society
Department of Neuroscience, University of Pennsylvania, Philadelphia, Pennsylvania 19104-6058
Freed, Michael A.
Rate of Quantal Excitation to a Retinal Ganglion Cell Evoked by
Sensory Input. J. Neurophysiol. 83: 2956-2966, 2000. To determine the rate and statistics of light-evoked
transmitter release from bipolar synapses, intracellular recordings
were made from ON-alpha ganglion cells in the periphery of
the intact, superfused, cat retina. Sodium channels were blocked with
tetrodotoxin to prevent action potentials. A light bar covering the
receptive field center excited the bipolar cells that contact the alpha cell and evoked a transient then a sustained depolarization. The sustained depolarization was quantified as change in mean voltage (
v), and the increase in voltage noise that
accompanied it was quantified as change in voltage variance
(
2). As light intensity increased,
v and 2 both increased, but their
ratio held constant. This behavior is consistent with Poisson arrival
of transmitter quanta at the ganglion cell. The response component
attributable to glutamate quanta from bipolar synapses was isolated by
application of 6-cyano-7-nitroquinoxaline (CNQX). As CNQX concentration
increased, the signal/noise ratio of this response component
(vCNQX/CNQX)
held constant. This is also consistent with Poisson arrival and
justified the application of fluctuation analysis. Two different
methods of fluctuation analysis applied to
vCNQX and CNQX produced
similar results, leading to an estimate that a just-maximal sustained
response was caused by ~3,700 quanta s
1. The transient
response was caused by a rate that was no more than 10-fold greater.
Because the ON-alpha cell at this retinal locus has
~2,200 bipolar synapses, one synapse released ~1.7 quanta s1 for the sustained response and no more than 17 quanta
s1 for the transient. Consequently, within the ganglion
cell's integration interval, here calculated to be ~16 ms, a bipolar
synapse rarely releases more than one quantum. Thus for just-maximal
sustained and transient depolarizations, the conductance modulated by a single bipolar cell synapse is limited to the quantal conductance (~100 pS at its peak). This helps preserve linear summation of quanta. The
v/2
ratio remained constant even as the ganglion cell's response saturated, which suggested that even at the peak of sensory input, summation remains linear, and that saturation occurs before the bipolar synapse.
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